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New motifs within the NB-ARC domain of R proteins: probable mechanisms of integration of geminiviral signatures within the host species of fabaceae family and implications in conferring disease resistance. (English) Zbl 1451.92244
Summary: The gemini viruses are a group of plant infectious agents, of which mungbean yellow mosaic India virus (MYMIV) belongs to the bipartite subgroup of gemini virus and causes serious yield penalty in the leguminous group of plants. In this investigation we have isolated two resistant gene homologues (RGHs; AY301990, AY301991) from two MYMIV-resistant lines of Vigna mungo and V. radiata that have high homology with a MYMIV-resistant linked marker, VMYR1 (AY 297425). These three resistance factors also have similarity with 221 reported \(R\) gene/RGH sequences in the NB-ARC domain of the family fabaceae. NB-ARC domain is an ancient, highly conserved domain of a class of plant disease resistance genes/proteins. Out of 221 in silico translated protein sequences, multialignment of 188 sequences without large insertion or truncation, unlike that of the rest 33, illustrated presence of both TIR and non-TIR subfamilies of NB-ARC domain. A critical analysis of these sequences revealed eight new conserved motifs, in addition to the reported conserved motifs within the NB-ARC domains, which are hitherto not reported. Further analysis of these eight motifs with the aid of PRINTS and PROSITE databases revealed signatures of geminiviral coat protein (GVCP) within the favoured allele, \(R\) gene or RGHs. GVCP signatures are absent within the NB-ARC domain of three species of Medicago, which are non-host to gemini virus. These observations tempted us to predict probable mechanism of integration of GVCP within the plant \(R\) gene/RGHs and their implications in conferring geminiviral disease resistance to the host plants. Our conjecture is that these signatures were integrated during plant pathogen interaction and are being maintained within this conserved domain through active selection of the favoured allele. We comprehensively addressed the biological significance of GVCP signatures, which probably provides additional defense against gemini viruses through degradation of homologous transcript of the virus.
MSC:
92D20 Protein sequences, DNA sequences
92C80 Plant biology
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[1] Aarts, N.; Metz, M.; Holub, E.; Staskawicz, B. J.; Daniels, M. J., Different requirements for EDS1 and NDR1 by disease resistance genes defined at least two \(R\) gene-mediated signaling pathways in Arabidopsis, Proc. Natl Acad. Sci. USA, 95, 10306-10311 (1998)
[2] Altschul, S. F.; Madden, T. L.; Schäffer, A. A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D. J., Gapped BLAST and PSI-BLAST: a new generation of protein database search pro-grams, Nucleic Acids Res., 25, 3389-3402 (1997)
[3] Attwood, T. K.; Mitchell, A.; Gaulton, A.; Moulton, G.; Tabernero, L., The PRINTS protein fingerprint database: functional and evolutionary applications, (Dunn, M.; Jorde, L.; Little, P.; Subramaniam, A., Encyclopaedia of Genomics, Proteomics and Bioinformatics (2006), Wiley: Wiley New York)
[4] Baker, B.; Zambryski, P.; Staskawicz, B.; Dinesh-Kumar, S. P., Signaling in plant-microbe interactions, Science, 276, 726-733 (1997)
[5] Basak, J.; Kundagrami, S.; Ghose, T. K.; Pal, A., Development of yellow mosaic virus (YMV) resistance linked DNA marker in Vigna mungo from populations segregating for YMV-reaction, Mol. Breed., 14, 375-383 (2004)
[6] Baulcombe, D. C., Mechanisms of pathogen-derived resistance to viruses in transgenic plants, Plant Cell, 8, 1833-1844 (1996)
[7] Bejarano, E. R.; Khashoggi, A.; Witty, M.; Lichtenstein, C., Integration of multiple repeats of geminiviral DNA into the nuclear genome of tobacco during evolution, Proc. Natl Acad. Sci., 93, 759-764 (1996)
[8] Brash, A. R., Lipoxygenases: occurrence, function, catalysis, and acquisition of substrate, J. Biol. Chem., 274, 23679-23682 (1999)
[9] Campbell, T. A., Investigation of variations in NBS motifs in alfalfa (Medicago sativa), M. edgeworthii and M. ruthenica, Can. J. Plant. Sci., 83, 371-376 (2003)
[10] Chellappan, P.; Masona1, M. V.; Vanitharani, R.; Taylor, N. J.; Fauquet, C. M., Broad spectrum resistance to ss DNA viruses associated with transgene-induced gene silencing in Cassava, Plant Mol. Biol., 56, 601-611 (2004)
[11] Day, A. G.; Bejarano, E. R.; Burrell, M.; Buck, K.; Lichtenstein, C., Expression of an antisense viral gene in transgenic tobacco confers resistance to the DNA virus tomato golden mosaic virus, Proc. Natl Acad. Sci., 88, 6721-6725 (1991)
[12] Dong, X.; van Wezel, R.; Stanley, J.; Hong, Y., Functional characterization of the nuclear localization signal for a suppressor of posttranscriptional gene silencing, J. Virol., 77, 7026-7033 (2003)
[13] Francisco, L.; Carlos, A. B.; Clara, S.-R.; Lucia, J.; Antonio, M., ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina, Plant J., 43, 165-180 (2005)
[14] Gorbunova, V. V.; Levy, A. A., How plants make ends meet: DNA double-strand break repair, Trends Plant Sci., 4, 263-269 (1999)
[15] Hammond-Kosack, K. E.; Jones, J. D.G., Plant disease resistance genes, Ann. Rev. Plant Physiol. Plant Mol. Biol., 48, 575-607 (1997)
[16] Hanley-Bowdoin, L.; Settlage, S. B.; Orozco, B. M.; Nagar, S.; Robertson, D., Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation, Crit. Rev. Plant Sci., 18, 71-106 (1999)
[17] Ilyina, T. V.; Koonin, E. V., Conserved sequence motifs in the initiator proteins for rolling circle DNA replication encoded by diverse replicons from eubacteria, eucaryotes and archaebacteria, Nucleic Acids Res., 20, 3279-3285 (1992)
[18] Kanazin, V.; Marek, L. F.; Shoemaker, R. C., Resistance gene analogs are conserved and clustered in soybean, Proc. Natl Acad. Sci. USA, 93, 11746-11750 (1996)
[19] Koonin, E. V.; Ilyina, T. V., Geminivirus replication proteins are related to prokaryotic plasmid rolling circle DNA replication initiator proteins, J. Gen. Virol., 73, 2763-2766 (1992)
[20] Leister, D.; Ballvora, A.; Salamini, F.; Gebhardt, C. A., PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants, Nat. Genet., 4, 421-429 (1996)
[21] Lucioli, A.; Noris, E.; Brunetti, A.; Tavazza, R.; Ruzza, V.; Castillo, A. G.; Bejarano, E. R.; Accotto, G. P.; Tavazza, M., Tomato yellow leaf curl Sardinia virus rep-derived resistance to homologous and heterologous geminiviruses occurs by different mechanisms and is overcome if virus-mediated transgene silencing is activated, J. Virol., 77, 6785-6798 (2003)
[22] Lupas, A., Coiled coils: new structures and new functions, Trends Biochem. Sci., 21, 375-382 (1996)
[23] Maccarone, M.; van Zadelhoff, G.; Veldink, G. A.; Vliegenthart, J. F.G.; Finazzi-Agrò, A., Early activation of lipoxygenase in lentil (Lens culinaris) root protoplasts by oxidative stress induces programmed cell death, Eur. J. Biochem., 267, 5078-5084 (2000)
[24] Mayo, M. A., Changes to virus taxonomy 2004, Arch. Virol., 150, 189-198 (2005)
[25] Meyers, B. C.; Dickerman, A. W.; Michelmore, R. W.; Sivaramakrishnan, S.; Sobral, B. W.; Young, N. D., Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily, Plant J., 3, 317-332 (1999)
[26] Niu, Q.-W.; Shih-Shun; Lin, S.-S.; Reyes, J. L.; Chen, K. C.; Wu, H.-W.; Yeh, S.-D.; Chua, N.-H., Expression of artificial microRNAs in transgenic Arabidopsis thaliana confers virus resistance, Nature Biotech., 24, 1420-1428 (2006)
[27] Pan, Q.; Wendel, J.; Fluhr, R., Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes, J. Mol. Evol., 50, 203-213 (2000)
[28] Pandey, S.; Assmann, S. M., The Arabidopsis putative G protein-coupled receptor GCR1 interacts with the G protein \(\alpha \)-subunit GPA1 and regulates abscisic acid signaling, Plant Cell, 16, 1616-1632 (2004)
[29] Pang, S.-Z.; Jan, F.-J.; Gonsalves, D., Nontarget DNA sequences reduce the transgene length necessary for RNA-mediated tospovirus resistance in transgenic plants, Proc. Natl Acad. Sci. USA, 94, 8261-8266 (1997)
[30] Puchta, H., The repair of double-strand breaks in plants: mechanisms and consequences for genome evolution, J. Exp. Bot., 56, 1-14 (2005)
[31] Raghavan, V.; Malik, P. S.; Choudhury, N. R.; Mukherjee, S. K., The DNA-A component of a plant geminivirus (Indian mung bean yellow mosaic virus) replicates in budding yeast cells, J. Virol., 78, 2405-2413 (2004)
[32] Rogers, S. G.; Bisaro, D. M.; Horsch, R. B.; Fraley, R. T.; Hoffmann, N. L.; Brand, L.; Elmer, J. S.; Lloyd, A. M., Tomato golden mosaic virus A component DNA replicates autonomously in transgenic plants, Cell, 45, 593-600 (1986)
[33] Salomon, S.; Puchta, H., Capture of genomic and T-DNA sequences during double-strand break repair in somatic plant cells, EMBO J., 17, 6086-6095 (1998)
[34] Sanford, J. C.; Johnston, S. A., The concept of parasite-derived resistance-deriving resistance genes from the parasités own genome, J. Theor. Biol., 113, 395-405 (1985)
[35] Seal, S. E.; vandenBosch, F.; Jeger, M. J., Factors influencing Begomovirus evolution and their increasing global significance: implications for sustainable control, Crit. Rev. Plant Sci., 25, 23-46 (2006)
[36] Shah, J., Lipids, lipases and lipid-modifying enzymes in plant disease resistance, Annu. Rev. Phytopathol., 43, 229-260 (2005)
[37] Shalev, G.; Levy, A. A., The maize transposable element Ac-induces recombination between the donor site and a homologous ectopic sequence, Genetics, 146, 1143-1151 (1997)
[38] Sigrist, C. J.A.; Cerutti, L.; Hulo, N.; Gattiker, A.; Falquet, L.; Pagni, M.; Bairoch, A.; Bucher, P., PROSITE: a documented database using patterns and profiles as motif descriptors, Brief Bioinform., 3, 265-274 (2002)
[39] Stanley, J.; Gay, M. R., Nucleotide sequence of cassava latent virus DNA, Nature, 301, 260-262 (1983)
[40] Sunter, G.; Bisaro, D. M., Transactivation of geminivirus AR1 and BR1 gene expression by the viral AL2 gene product occurs at the level of transcription, Plant Cell, 4, 1321-1331 (1992)
[41] Sunter, G.; Gardiner, W. E.; Rushing, A. E.; Rogers, S. G.; Bisaro, D. M., Independent encapsidation of tomato golden mosaic virus A component DNA in transgenic plants, Plant Mol. Biol., 8, 477-484 (1987)
[42] Thompson, J. D.; Higgins, D. G.; Gibson, T. J., CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighing, position-specific gap penalties and weight matrix choice, Nucleic Acids Res., 22, 4673-4680 (1994)
[43] van der Biezen, E. A.; Jones, J. D.G., The NB-ARC domain: a novel signaling motif shared by plant resistance gene products and regulators of cell death in animals, Curr. Biol., 8, 226-227 (1998)
[44] Vanitharani, K.; Chellappan, P.; Fauquet, C. M., Geminiviruses and RNA silencing, Trends Plant Sci., 10, 144-151 (2005)
[45] Varsani, A.; Williamson, A.-L.; Rose, R. C.; Jaffer, A.; Rybicki, E. P., Expression of human papillomavirus type 16 major capsid protein in transgenic Nicotiana tabacum cv, Xanthi. Arch. Virol., 148, 1771-1786 (2003)
[46] Veronico, P.; Giannino, D.; Teresa Melillo, M.; Leone, A.; Reyes, A.; Kennedy, M. W.; Bleve-Zacheo, T., A novel lipoxygenase in pea roots. Its function in wounding and biotic stress, Plant Physiol., 141, 1045-1055 (2006)
[47] Voinnet, O.; Pinto, Y. M.; Baulcombe, D. C., Suppression of gene silencing: A general strategy used by diverse DNA and RNA viruses of plants, Proc. Natl Acad. Sci. USA, 96, 14147-14152 (1999)
[48] Wasternack, C.; Miersch, O.; Kramell, R.; Hause, B.; Ward, J.; Beale, M.; Boland, W.; Parthier, B.; Feussner, I., Jasmonic acid-biosynthesis, signal transduction, gene expression, Fett. Lipid, 100, 139-146 (1998)
[49] Young, N. D., The genetic architecture of resistance, Curr. Opin. Plant Biol., 3, 285-290 (2000)
[50] Yu, Y. G.; Buss, G. R.; Maroof, M. A., Isolation of a superfamily of candidate disease-resistance genes in soybean based on a conserved nucleotide-binding site, Proc. Natl Acad. Sci. USA, 93, 11751-11756 (1996)
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